Estimating information in time-varying signals

PLoS Comput Biol. 2019 Sep 3;15(9):e1007290. doi: 10.1371/journal.pcbi.1007290. eCollection 2019 Sep.

Abstract

Across diverse biological systems-ranging from neural networks to intracellular signaling and genetic regulatory networks-the information about changes in the environment is frequently encoded in the full temporal dynamics of the network nodes. A pressing data-analysis challenge has thus been to efficiently estimate the amount of information that these dynamics convey from experimental data. Here we develop and evaluate decoding-based estimation methods to lower bound the mutual information about a finite set of inputs, encoded in single-cell high-dimensional time series data. For biological reaction networks governed by the chemical Master equation, we derive model-based information approximations and analytical upper bounds, against which we benchmark our proposed model-free decoding estimators. In contrast to the frequently-used k-nearest-neighbor estimator, decoding-based estimators robustly extract a large fraction of the available information from high-dimensional trajectories with a realistic number of data samples. We apply these estimators to previously published data on Erk and Ca2+ signaling in mammalian cells and to yeast stress-response, and find that substantial amount of information about environmental state can be encoded by non-trivial response statistics even in stationary signals. We argue that these single-cell, decoding-based information estimates, rather than the commonly-used tests for significant differences between selected population response statistics, provide a proper and unbiased measure for the performance of biological signaling networks.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium Signaling / physiology
  • Computational Biology / methods*
  • MAP Kinase Signaling System / physiology
  • Mammals / physiology
  • Models, Biological*
  • Signal Transduction / physiology*
  • Single-Cell Analysis
  • Time Factors
  • Yeasts / physiology

Grant support

GT and SACH acknowledge the support of the Austrian Science Fund (https://fwf.ac.at/en/) grant FWF P28844. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.